Meta Analysis Journal

Cutaneous melanoma attributable to sunbed use:systematic review and meta-analysis

OPEN ACCESS

Mathieu Boniol director of research 1, Philippe Autier director of research 1, Peter Boyle president 1,Sara Gandini senior staff scientist 2

1International Prevention Research Institute, 95 cours Lafayette, 69006 Lyon, France; 2European Institute of Oncology, Milan, Italy

AbstractObjective To estimate the burden of melanoma resulting from sunbeduse in western Europe.

Design Systematic review and meta-analysis.

Data sources PubMed, ISI Web of Science (Science Citation IndexExpanded), Embase, Pascal, Cochrane Library, LILACS, and MedCarib,along with published surveys reporting prevalence of sunbed use atnational level in Europe.

Study selection Observational studies reporting a measure of risk forskin cancer (cutaneousmelanoma, squamous cell carcinoma, basal cellcarcinoma) associated with ever use of sunbeds.

Results Based on 27 studies ever use of sunbeds was associated witha summary relative risk of 1.20 (95% confidence interval 1.08 to 1.34).Publication bias was not evident. Restricting the analysis to cohorts andpopulation based studies, the summary relative risk was 1.25 (1.09 to1.43). Calculations for dose-response showed a 1.8% (95% confidenceinterval 0% to 3.8%) increase in risk of melanoma for each additionalsession of sunbed use per year. Based on 13 informative studies, firstuse of sunbeds before age 35 years was associated with a summaryrelative risk of 1.87 (1.41 to 2.48), with no indication of heterogeneitybetween studies. By using prevalence data from surveys and data fromGLOBOCAN 2008, in 2008 in the 15 original member countries of theEuropean Community plus three countries that were members of theEuropean Free Trade Association, an estimated 3438 cases of melanomacould be attributable to sunbed use, most (n=2341) occurring amongwomen.

Conclusions Sunbed use is associated with a significant increase inrisk of melanoma. This risk increases with number of sunbed sessionsand with initial usage at a young age (<35 years). The cancerous damageassociated with sunbed use is substantial and could be avoided by strictregulations.

IntroductionExposure to the sun is the most important environmental causeof skin cancer, with the wavelength for ultraviolet radiationassociated with development of the disease.1 The wavelengths

for ultraviolet radiation range between 100 nm and 400 nm andare broadly categorised into ultraviolet A light (315-400 nm),ultraviolet B (280-315 nm), and ultraviolet C (100-280 nm).All ultraviolet C andmost ultraviolet B wavelengths are blockedby the stratospheric ozone layer. A fraction of ultraviolet B andall ultraviolet A reaches the Earth’s surface.In light skinned populations, the ultraviolet radiation deliveredby sunbeds has become the main non-solar source of exposureto ultraviolet light. Indoor tanning has been widely practised innorthern Europe and the United States since the 1980s,2 andsince 2000 this trend has gained popularity in sunnier countries,such as Australia.3 4 Modern indoor tanning equipment mainlyemits in the ultraviolet A range, but a fraction (<5%) of thisspectrum is in the ultraviolet B range. This ultraviolet B fractioninduces a deep, long lasting tan. Powerful ultraviolet tanningunits may be 10-15 times stronger than the midday sunlight ontheMediterranean Sea, and repeated exposure to large amountsof ultraviolet A delivered to the skin in relatively short periods(typically 10-20 minutes) constitutes a new experience forhumans.Indoor tanning has a plethora of negative health effects, manyof which are involved in cancerous processes.5 The impact ofthis trend on incidence of skin cancer is of concern, mainlybecause of cutaneous malignant melanoma, a cancer of poorprognosis when diagnosed at an advanced stage.Until recently ultraviolet B was usually considered the onlycarcinogenic fraction of the solar spectrum reaching the Earth’ssurface. In 2009, the International Agency for Research onCancer classified the whole ultraviolet spectrum and indoortanning devices as carcinogenic to humans (group 1).6 Therationale for classifying ultraviolet A and sunbeds as group 1carcinogens was based on congruent lines of evidence frombasic and epidemiological research. Briefly, extensive laboratorydata and animal experiments (on DNA mutations and repair,immune function, cell integrity, cell cycle regulation, and othercritical biological functions) documented a role for ultravioletA in skin carcinogenesis7-9 and that the body’s repair and

Correspondence to: M Boniol [email protected]

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BMJ 2012;345:e4757 doi: 10.1136/bmj.e4757 (Published 24 July 2012) Page 1 of 12

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removal of damaged DNA was less effective when the damagewas caused by ultraviolet A rather than by ultraviolet B.10Experiments in human volunteers showed that exposure toultraviolet A and ultraviolet B can weaken the immune systemthrough mechanisms that interact and overlap, increasingvulnerability to cancer as well as to other diseases.11 Also,tanning lamps induce the types of DNA damage to the skinassociated with photocarcinogenesis.11 Lastly, the meta-analysisundertaken in 2005 found a significant 75% increase in risk ofmelanoma (from 40% to 228%) when indoor tanning startedduring adolescence or young adulthood.11 12 Some evidence wasalso found that indoor tanning increased the risk of squamouscell carcinoma, especially when sunbed use started before theage of 20.The meta-analysis by the International Agency for Research onCancer in 2006 could not examine dose-responses, andadditional epidemiological studies published since then haveprovided an opportunity for some aspects of the relation betweensunbed use andmelanoma to be explored in greater depth. Usingmeta-analysis we quantified the risk of melanoma associatedwith indoor tanning using artificial ultraviolet light, includingdose-response and the estimated burden of melanoma and deathassociated with sunbed use in western Europe.

MethodsTo update the meta-analysis of 2006, we used the samemethodological approach as previously described.11Briefly, MBsearched the literature published up to May 2012 using thedatabases PubMed, ISIWeb of Science (Science Citation IndexExpanded), Embase, Pascal, Cochrane Library, LILACS, andMedCarib. We used the following keywords for diseases: “skincancer”, “squamous cell carcinoma”, “SCC”, “basal cellcarcinoma”, “BCC”, and “melanoma”. To define exposure, weused the following keywords: “sunbed”, “sunlamp”, “artificialUV”, “artificial light”, “solaria”, “solarium”, “indoor tanning”,“tanning bed”, “tanning parlour”, “tanning salon”, and “tanningbooth”. No language restriction was applied. We reviewed thetitles and abstracts to identify potentially eligible studies andcarried out a manual search of studies identified from referencescited in reviews on skin cancer.From the initial search we selected case-control, cohort, andcross sectional studies published as original articles. Non-eligibletrials included ecological studies, case reports, reviews, andeditorials.PA and SG reviewed the selected articles and SG and MBabstracted the data using a standardised data collection protocol.The minimal common information on use of indoor tanningappliances for all studies was “ever used.” For those studies thatdid not strictly assess ever users of indoor tanning appliancescompared with never users,13 14we used the information closestto this category.We also extracted the highest category of sunbed use reportedin each study—that is, the greater duration (defined as “highuse”) along with estimates of risk for the association with firstuse of sunbeds at a young age—before age 35 years.

Statistical analysisWe transformed every measure of association, adjusted for themaximum number of confounding variables, and 95%confidence intervals, into logarithms of relative risk andcalculated the corresponding variance.15 When no estimateswere reported, we used tabular data to calculate the crudeestimates and 95% confidence intervals.

The meta-analysis was calculated from a random effect modelas described previously16—that is, a mixed effects model withsummary relative risk obtained from maximum likelihoodestimation. We calculated confidence intervals assuming anunderlying t distribution. Heterogeneity was assessed byHigginsand Thompson’s I2 statistic.17 The I2 statistic ranges from zeroto 100%, zero indicating that the relative risks of the differentstudies included in the meta-analysis are homogeneous—thatis, that the relative risks are consistent with each other.We used a two step procedure to obtain summary risk estimatesfor dose-response. Firstly, we fitted a linear model within eachstudy to estimate the relative risk per session of sunbed use.When sufficient information was published (the number ofparticipants in usage category), we fitted the model accordingto a previously proposed method.18 This method provides thenatural logarithm of the relative risk and an estimator of itsstandard error, taking into account that the estimates for separatecategories depend on the same reference group. When thenumbers of participants in each serum level category were notavailable from the publications, we calculated coefficientsignoring the correlation between the estimates of risk at theseparate exposure levels. Secondly, we estimated the summaryrelative risk by pooling the study specific estimates with themixed effects models.All analyses were done with SAS Windows version 9.2. Weused PROC MIXED in SAS to calculate the random effectsmodels.

Heterogeneity and sensitivity analysesWe carried out several sensitivity analyses to evaluate thestability of the pooled estimates. Firstly we examined the pooledrelative risks for case-control and prospective (cohort and nestedcase-control) studies separately. Then we examined changes tothe results after the exclusion of specific studies.To investigate heterogeneity between the studies we carried outmetaregressions and subgroup analyses. Heterogeneity wasinvestigated by looking at factors that could influence the qualityof the studies and that could be responsible for heterogeneity,such as the study design, adjustment for confounding factors,features of the population, and publication year. As an additionalanalysis for heterogeneity, we compared risk estimates accordingto the average latitude of countries or areas where studies weredone.To investigate whether publication bias may have affected thevalidity of the estimates, we constructed funnel plots of theregression of log relative risk on the sample size, weighted bythe inverse of the pooled variance. We evaluated publicationbias using the Macaskill test.19

Sunbed use and burden of melanomaTo translate the estimation of risk in the current study to theburden in the general population, we provided a broad estimationof the burden of sunbed use in Europe. We gathered data on theprevalence of sunbed use from recent surveys carried out inEurope. As no survey was available for central Europeancountries, we limited our estimation to the original 15 countriesof the European Community (Austria, Belgium, Denmark,Finland, France, Germany, Greece, Ireland, Italy, Luxembourg,Spain, Sweden, Portugal, the Netherlands, and the UnitedKingdom) plus the three countries that are part of the EuropeanFree Trade Association (Iceland, Norway, and Switzerland).For these 18 countries, we extracted data on the incidence ofmelanoma from GLOBOCAN 2008.20



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We identified seven surveys carried out in the 18 countries fromwhich we extracted prevalence of ever having used a sunbedduring lifetime.21-27 We also extracted the prevalence of sunbeduse in the control group included in the Swedish cohort.14 Datawere available for Denmark, France, Germany, Iceland, Spain,Sweden, Switzerland, and the United Kingdom. These countriesrepresent 70% of all melanoma cases occurring in the 18countries studied. Prevalence for the other 10 countries wasdetermined from estimates for neighbouring countries.We estimated the attributable fraction with Levin’s formula28by using prevalence of ever use of sunbeds from surveys andthe summary relative risk for ever use of sunbeds.

ResultsFigure 1⇓ describes the literature search process. Since themeta-analysis of 2006, eight additional studies were identified,one of which was the update of the Norwegian-Swedish cohort.29Thus in May 2012, 32 studies had investigated the relationbetween sunbed use and melanoma (table 1⇓). All studies werebased on the case-control design except three, which were cohortstudies.14 50 59 The Nurse’s Health Study was based on a cohortdesign but the trial was a case-control study with retrospectiveassessment of sun exposure and sunbed use in samples of skincancer cases and controls matched on year of birth.42One studywas a survey among patients attending a dermatology clinic.53One third of patients participated in the survey. Sunbed use ofpatients with a diagnosis of cutaneous melanoma was comparedwith that of other patients. Although this study was not in thebroadest sense a case-control design, it was included in themeta-analysis.Four of the 32 studies13 14 30-59 were excluded from themeta-analysis because they did not include estimates of therelative risk for cutaneous melanoma associated with sunbeduse.34 44 46 40One study55was redundant as it was reanalysed andpublished in 1999.54

Studies used for meta-analysis totalled 11 428 cases ofmelanoma. The first study30was published in 1981 and the last59in 2012. Eighteen studies were carried out in European countries,seven in the United States and Canada, and two in Australia.

Summary relative risksTwenty seven studies presented positive estimates for ever usecompared with never use of sunbeds (fig 2⇓). Eight of thesestudies reported only crude relative risks and one adjusted forage and sex only. The summary relative risk was 1.20 (95%confidence interval 1.08 to 1.34), with heterogeneity (I2=56%).Evidence of publication bias was lacking (P=0.99, Macaskilltest). An analysis restricted to the 18 cohort and populationbased case-control studies produced a slightly higher summaryrelative risk (1.25, 1.09 to 1.43). An analysis restricted to the18 studies that adjusted for confounders related to sun exposureand sun sensitivity yielded a similar summary relative risk (1.29,1.13 to 1.48).When the cohort studies were excluded from the analysis thesummary relative risk decreased slightly but remainedstatistically significant (1.20, 1.06 to 1.37).Thirteen studies presented estimates relevant for the evaluationof first use of sunbeds in youth (before age 35) compared withnever use (fig 3⇓). All relative risks were adjusted forconfounders related to sun exposure or sun sensitivity, exceptin one study.54 The risk was almost doubled (relative risk 1.87),with no indication of heterogeneity (I2=0).

Four studies reported data on risk associated with the numberof sunbed sessions per year. A summary relative risk derivedfrom relative risks reported for each session was 1.018 (95%confidence interval 0.998 to 1.038), which indicated a 1.8%increase in risk of melanoma for each annual session. Asignificant 42% increased risk was found for high use of sunbeds(summary relative risk 1.42, 95% confidence interval 1.15 to1.74; fig 4⇓). Nine studies reported risks associated with timesince first use, with first use distant in time (that is, more thanfive years before diagnosis) associated with a higher summaryrelative risk (1.49, 1.18 to 1.88; I2=34%) than first use morerecently (1.18, 0.95 to 1.48; I2=51%, table 2⇓).Risks for sunbed related melanoma were compared inpopulations living at different latitudes (fig 5⇓). Relative risksassociated with ever versus never use of sunbeds did not differmuch with variations in latitude and there was no indicationthat risks would be higher in more sun sensitive populationssuch as those in the Nordic countries.

Sensitivity analysisThe summary relative risk remained significant when all possiblestudies, including publications with missing estimates, wereincluded and a relative risk of 1 (no effect) was imputed for themissing relative risks (1.20, 1.10 to 1.34).

Squamous and basal cell carcinomasTwo studies42 59 published since 2005 looked at the risk ofnon-melanoma skin cancer associated with sunbed use. Addingdata from this study to that of the 2006 meta-analysis11 yieldedsummary relative risks for ever versus never sunbed use of 2.23(1.39 to 3.57) for squamous cell carcinoma (1242 cases in fivestudies)42 59-62 and 1.09 (1.01 to 1.18) for basal cell carcinoma(6995 cases in six studies).42 59 61-64

Impact on burden of melanoma in westernEuropeOf 63 942 new cases of cutaneous melanoma diagnosed eachyear in the 15 countries that were members of the EuropeanCommunity and the three countries that were part of theEuropean Free Trade Association, an estimated 3438 (5.4%)were related to sunbed use (table 3⇓).Women represented mostof this burden, with 2341 cases (6.9% of all melanoma cases inwomen) related to sunbed use; 1096 cases annually occurred inmen (3.7% of all cases in men). Taking a melanoma incidenceto mortality ratio of 3.7 for European men and 4.7 for Europeanwomen,20 in the 15 European Community countries, about 498women and 296 men would die each year from a melanoma asa result of being exposed to indoor tanning using artificialultraviolet light.

DiscussionOverall, the summary of results of 27 observational studiespublished within the past 30 years shows that the risk ofcutaneous melanoma is increased by 20% for those who wereever users of indoor tanning devices with artificial ultravioletlight. The risk of melanomawas doubled when use started beforethe age of 35 years. This latest estimate originates from studiesin various populations and latitudes, which obtained consistentresults with zero heterogeneity. Summary risk estimatescalculated from population based case-control studies were closeto those of cohort studies.



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Comparison with 2006 evaluationThe 2006 evaluation11 did not find evidence for a dose-responserelation between the level of sunbed use and risk of melanoma;however, a formal metaregression analysis could not be carriedout because not enough data were published at that time. Sincethen, large studies have provided data consistent with adose-response relation—for example, a study in Minnesota47found dose-responses for years during which sunbeds were used,cumulative time (hours) of sunbed use, and cumulative numberof tanning sessions.Table 2 summarises the results of the meta-analyses of 200611and of this meta-analysis. From 2005 to 2011, most summaryrelative risks have increased. These changes support thehypothesis that earlier studies tended to underestimate risksassociated with indoor tanning because this behavioural trendis relatively new and thus recent uses may not (yet) haveinfluenced the incidence of melanoma.11 65 From this logic it ispossible that future epidemiological studies on sunbed use andskin cancer could show relative risks higher than those foundto date.

Risk of melanoma associated with sunbeduse in different populationsWe did not observe a significant difference in risk when takinglatitude of residence into account. Most studies included in thismeta-analysis were adjusted for phototype or a proxy for sunsensitivity. In this respect, the summary relative risks presentedin this article are valid for all light skinned populations such asthose in Europe, North America, and Australasia. The numberof melanoma cases arising from sunbed use may, however, behigher than we estimated because it seems that sunbed users aremore likely to have fair skin, have red or blond hair, have morefreckles, and be phototype I/II (burn easily and tan minimallyif at all when first exposed to the sun) than III/IV (burnmoderately and tan easily or always when first exposed to thesun) than non-users.66

Sunbed users also have the tendency to adopt unhealthylifestyles compared with non-users2 and we could hypothesisethat use of sunbeds may be a marker of populations moreexposed to sun. However, several studies, such as the cohortstudy by Veierød et al14 (see table 1), did adjust for a variableof sun exposure. The summary relative risk is then unlikely toreflect a more intense exposure to sun among sunbed users.Compelling evidence that use of sunbeds can be a cause ofmelanoma and not just a proxy for sun exposure arises from theinvestigation of a melanoma epidemic in Iceland, a countrylocated between 64° and 66° N and where sunny days areuncommon.67After 1990, the incidence of melanoma increasedsharply, mainly in young women, with preferential occurrenceon the trunk. The incidence tended to decline after 2000, whenpublic health authorities imposed greater control on sunbedinstallation and utilisation. Although that study was anecological one, the exposure of Icelandic youngsters that tookplace after 1985 seemed to be the most likely reason for thatepidemic.68

The results of this meta-analysis are in full agreement with theconsiderable amount of data pointing to childhood andadolescence as the key periods for initiation and developmentof melanoma in adulthood.69 This evidence on the risks of skincancer associated with exposure to ultraviolet light at youngages underlines the health threats documented by many recentsurveys, which show substantial use by children and adolescentsof tanning devices using artificial ultraviolet light in the UnitedStates and European countries,70-73 with evidence for unabated

increasing use in the United States.74 For instance, in Denmark,a survey completed in 2008 found that 2% of children aged 8to 11 years and 13% aged 12 to 14 years had used a sunbedwithin the past 12 months.72

Burden ofmelanoma associatedwith sunbeduse in EuropeIn Europe, 71% of melanoma cases in 2008 occurred in the 15European Union countries and the three European Free TradeAssociation countries. We estimated that in these 18 countrieseach year, around 3438 new cases of melanoma and 794 relateddeaths would be related to sunbed use. This estimation is limitedto western European countries because of a lack of informationon sunbed use in central European countries. The number ofdeaths from melanoma associated with sunbed use wasdetermined for the United Kingdom in 2003,75with an estimated100 deaths (range 50-200) annually. Our calculation ofattributable fractions would put the number of deaths for theUnited Kingdom at 99, a figure consistent with the earlierestimate. The estimation of deaths from melanoma should betreated with caution since some epidemiological data suggestthat, on average, sunbed related melanoma could be of lowmalignant potential.75 76 None the less, the burden of cancerattributable to sunbed use could further increase in the next 20years because the recent, high usage levels observed in manycountries have not yet achieved their full carcinogenic effectand because usage levels of teenagers and young adults remainhigh in many countries. This prediction is supported by theobservation over 10-15 years of increases in the incidence ofmelanoma on the trunks of women from countries withwidespread access to indoor tanning.67 77-80 The incidence ratesof trunk melanoma in women aged 20-49 years therefore couldbe a relevant indicator for monitoring activities to decrease theuse of sunbeds.

Indoor tanning industry and regulationMelanoma and other skin cancers that are specifically associatedwith sunbed use are preventable diseases by avoiding exposureto these devices. Generally the sunbed industry has not selfregulates effectively and has tended to disseminate non-evidencebased information, which can deceive consumers.81-83 Tanningsalon operators simply following regulations is an illusoryprevention method, as such regulations are unable to turn acarcinogenic agent into a healthy one. Instead, the sunbedindustry has used the opportunity to claim that properlyregulated indoor tanning is safe, and that it might even havehealth benefits.81

Discouraging sunbed use or requiring parental authorisation isnot effective, partly because many parents of teenagers willingto use sunbeds are also sunbed users themselves.2 73

Prevention of the harmful effects associated with sunbed usemust be based on tougher actions. Recommendations from theWorld Health Organization, the International Commission onNon-Ionizing Radiation Protection (ICNIRP), and the EuropeanSociety of Skin Cancer Prevention (EUROSKIN) maintain thatthe highest regulatory priorities should be the restriction ofsunbed use by people under 18 years of age and the banning ofunsupervised indoor tanning facilities. Such restrictions havenow been implemented in Australia and in several Europeancountries (Austria, Belgium, France, Germany, Portugal,Scotland, and Spain). In the United States, until the recent banby the state of California issued on 10 October 2011, no statehad banned access to indoor tanning for adolescents aged lessthan 18 years.



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If sunbed use by teenagers and young adults does notsubstantially decrease in the short term, thenmore radical actionsshould be envisioned, such as the nationwide prohibition of thepublic use of tanning devices, which was implemented by theBrazilian National Health Surveillance Agency84 in November2009.85

Contributors: MB, SG, and PA carried out the literature search andextracted data. MB and SG did the statistical analysis and drafted thefirst manuscript. All authors interpreted the data, contributed todiscussion, and reviewed or edited the manuscript. All authors takeresponsibility for the integrity of the data and the accuracy of the dataanalysis and are guarantors for the paper.Competing interests: All authors have completed the ICMJE uniformdisclosure form at www.icmje.org/coi_disclosure.pdf (available onrequest from the corresponding author) and declare: no support fromany organisation for the submitted work; no financial relationships withany organisations that might have an interest in the submitted work inthe previous three years; and no other relationships or activities thatcould appear to have influenced the submitted work.Ethical approval: Not required.Data sharing: The statistical analysis programs in SAS are available onrequest from the corresponding author ([email protected]).

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http://www.icmje.org/coi_disclosure.pdf

http://www.inpes.fr



What is already known on this topic

Earlier studies suggested an increased risk of melanoma, in particular when sunbed use started before age 35No consistent dose-response relation was found

What this study adds

This study confirms a doubling of the risk of melanoma when first sunbed use is at a young age (<35 years)A dose-response relation exists between amount of sunbed use and risk of melanomaIn Europe each year, 3438 new cases of melanoma would be due to sunbed use

62 Karagas MR, Stannard VA, Mott LA, Slattery MJ, Spencer SK, Weinstock MA. Use oftanning devices and risk of basal cell and squamous cell skin cancer. J Natl Cancer Inst2002;94:224-6.

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64 Walther U, Kron M, Sander S, Sebastian G, Sander R, Peter RU, et al. Risk and protectivefactors for sporadic basal cell carcinoma: results of a two-centre case-control study insouthern Germany. Clinical actinic elastosis may be a protective factor. Br J Dermatol2004;151:170-8.

65 Autier P. Perspectives in melanoma prevention: the case of sunbeds. Eur J Cancer2004;40:2367-76.

66 Ezzedine K, Malvy D, Mauger E, Nageotte O, Galan P, Hercberg S, et al. Artificial andnatural ultraviolet radiation exposure: beliefs and behaviour of 7200 French adults. J EurAcad Dermatol Venereol 2008;22:186-94.

67 Héry C, Tryggvadóttir L, Sigurdsson T, Sigurdsson T, Ólafsdóttir E, Sigurgeirsson B, etal. A melanoma epidemic in Iceland: possible influence of sunbed use. Am J Epidemiol2010;172:762-7.

68 Alberg AJR. A melanoma epidemic in Iceland: possible influence of sunbed use. Am JEpidemiol 2011;173:845.

69 Autier P, Boyle P. Artificial ultraviolet sources and skin cancers: rationale for restrictingaccess to sunbed use before 18 years of age. Nat Clin Pract Oncol 2008;5:178-9.

70 Cokkinides V, Weinstock M, Lazovich D, Ward E, Thun M. Indoor tanning use amongadolescents in the US, 1998 to 2004. Cancer 2009;115:190-8.

71 Guy GP, Tai E, Richardson LC. Use of indoor tanning devices by high school studentsin the United States, 2009. Prev Chronic Dis 2011;8:A116.

72 Krarup AF, Koster B, Thorgaard C, Philip A, Clemmensen IH. Sunbed use by childrenaged 8-18 years in Denmark in 2008: a cross-sectional study. Br J Dermatol2011;165:214-6.

73 Mayer JA, Woodruff SI, Slymen DJ, Sallis JF, Forster JL, Clapp EJ, et al. Adolescents’use of indoor tanning: a large-scale evaluation of psychosocial, environmental, andpolicy-level correlates. Am J Public Health 2011;101:930-8.

74 Buller DB, Cokkinides V, Hall I, Hartman AM, Saraiya M, Miller E, et al. Prevalence ofsunburn, sun protection, and indoor tanning behaviors among Americans: review fromnational surveys and case studies of 3 states. J Am Acad Dermatol 2011;65:S114-23.

75 Diffey B. A quantitative estimate of melanoma mortality from ultraviolet A sunbed use inthe UK. Br J Dermatol 2003;149:578-81.

76 Autier P, Doré JF, Eggermont AMM, Coebergh JW. Epidemiological evidence that theUVA radiation is involved in the genesis of cutaneous melanoma. Curr Opin Oncol2011;23:189-96.

77 Bradford PT, Anderson WF, Purdue MP, Goldstein AM, Tucker MA. Rising melanomaincidence rates of the trunk among younger women in the United States.Cancer EpidemiolBiomarkers Prev 2010;19:2401-6.

78 Dal H, Boldemann C, Lindelöf B. Does relative melanoma distribution by body site1960-2004 reflect changes in intermittent exposure and intentional tanning in the Swedishpopulation? Eur J Dermatol 2007;17:428-34.

79 Mowbray M, Stockton DL, Doherty VR. Changes in the site distribution of malignantmelanoma in South East Scotland (1979-2002). Br J Cancer 2007;96:832-5.

80 Montella A, Gavin A, Middleton R, Autier P, Boniol M. Cutaneous melanoma mortalitystarting to change: a study of trends in Northern Ireland. Eur J Cancer 2009;45:2360-6.

81 Autier P, Doré JF, Breitbart E, Greinert R, Pasterk P, Boniol M. The indoor tanningindustry’s double game. Lancet 2011;377:1299-301.

82 Federal Trade Commission. Indoor tanning. FTC consumer alert, March 2010. www.ftc.gov/bcp/edu/pubs/consumer/alerts/alt174.pdf.

83 Greenman J, Jones DA. Comparison of advertising strategies between the indoor tanningand tobacco industries. J Am Acad Dermatol 2010;62:685,e1-18.

84 ANVISA. Agência Nacional de Vigilância Sanitária Resolução No 59 de 9 de novembro2009. Proibe em todo território nacional o uso dos equipamentos para bronzeamentoartificial, com finalidade estética, baseada na emissão da radiação ultraviolet (UV). DiárioOficial da União—Seção 1, No 215, quarta-feira, 11 de novembro de 2009. www.saude.mg.gov.br/atos_normativos/legislacao-sanitaria/RESOLUCaO%20RDC%2056.pdf.

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Accepted: 2 July 2012

Cite this as: BMJ 2012;345:e4757This is an open-access article distributed under the terms of the Creative CommonsAttribution Non-commercial License, which permits use, distribution, and reproduction inany medium, provided the original work is properly cited, the use is non commercial andis otherwise in compliance with the license. See: http://creativecommons.org/licenses/by-nc/2.0/ and http://creativecommons.org/licenses/by-nc/2.0/legalcode.



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http://www.ftc.gov/bcp/edu/pubs/consumer/alerts/alt174.pdf

http://www.ftc.gov/bcp/edu/pubs/consumer/alerts/alt174.pdf

http://www.saude.mg.gov.br/atos_normativos/legislacao-sanitaria/RESOLUCaO%20RDC%2056.pdf

http://www.saude.mg.gov.br/atos_normativos/legislacao-sanitaria/RESOLUCaO%20RDC%2056.pdf

http://creativecommons.org/licenses/by-nc/2.0/

http://creativecommons.org/licenses/by-nc/2.0/

http://creativecommons.org/licenses/by-nc/2.0/legalcode



Tables

Table 1| Characteristics of studies on sunbed use and melanoma considered for meta-analysis

AdjustmentsNo of controlsNo of casesCountryStudies

Cohort or population based case-controlstudies:

Crude207169UKAdam et al 198130

—595595CanadaGallagher et al 198640*

Crude511511AustraliaHolman et al 198645

Not clear926474DenmarkOsterlind et al 198851

Age, hair colour, skin reaction, sunburn inchildhood, education level

416208ItalyZanetti et al 198858

—505523SwedenBeitner et al 199034*

—608583CanadaWalter et al 199055*†

Hair colour, nevi, skin type, sunburns640400SwedenWesterdahl et al 199457

—930452USAHolly et al 199543

Age, sex, phenotype, recreational sun exposure512624USAChen et al 199835

Age, sex, and skin reaction608583CanadaWalter et al 199954

Sunburns, hair colour, sunbathing913571SwedenWesterdahl et al 200056

804200USAHan et al 200642

Age, sex, family history, hair colour, sunexposure

678423USAClough-Gorr et al 200836

—479604AustraliaCust et al 201137

Age, sex, family history, hair colour, sunexposure

11011167USALazovich et al 201047

Age, residence, hair colour, sunburns, annual“bathing” holiday

106 366‡412Norway, SwedenVeierød et al 201014

Age, sex, educational level, family history ofmelanoma, sun sensitivity, and sun exposure

513959UKElliott et al 201139

Crude29 520‡210SwedenNielsen et al 201150

Age, family history, hair colour, number ofmoles, sunburn tendency and history, outdoorsun exposure, ultraviolet index, state ofresidence at birth, age 15, and age 30

73 494‡349USAZhang et al 201259

Other case-control studies:

—13178NorwayKlepp and Magnus 197946*

—139121USAHolly et al 198744*

Crude120180UKSwerdlow et al 198852

Nevi, skin type, sunburn, freckles, tropicalresidence

180280UKMacKie et al 198948

Crude100100UKDunn-Lane et al 199338

Nevi, hair type, and phototype§280280GermanyGarbe et al 199341

Crude447420MulticentreAutier et al 199431

Age, sex, skin, hair, eye, nevi, freckles,sunburns, number of holidays in sunny climates

538542ItalyNaldi et al 200049

Crude271271GermanyKaskel et al 200113

Sex and age416413UKBataille et al 200433

Sex, age, and skin phototype§622597Belgium, France,Netherlands, Sweden, UK

Bataille et al 200532

Not clear30729USATing et al 200753

*Not included in main meta-analysis as no estimate of risk was reported.†1990 study was reanalysed in 1999. Present meta-analysis uses relative risk adjusted for potential confounders presented in 1999 publication.‡Cohort size.



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Table 1 (continued)

AdjustmentsNo of controlsNo of casesCountryStudies

§Sensitivity to sunlight.



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Table 2| Summary relative risks found by meta-analyses on sunbed use and cutaneous melanoma

I2 (%)Summary relative risk (95% CI)No of studies in present

meta-analysisSummary relative risk (95%CI)No of studies in 2005

meta-analysis*Sunbed use

561.20 (1.08 to 1.34)271.15 (1.00 to 1.31)19Ever use

601.25 (1.09 to 1.43)181.17 (0.96 to 1.42)10Ever use†

01.87 (1.41 to 2.48)131.75 (1.35 to 2.26)7First use in youth (<35 years)

—1.42 (1.15 to 1.74)14NRNRHigh use

511.18 (0.95 to 1.48)91.10 (0.76 to 1.60)5First use recently

341.49 (1.18 to 1.88)91.49 (0.93 to 2.38)5First use distant in time‡

NR=not reported.*International Agency for Research on Cancer, 2006.†Cohort or population based case-control studies only.‡More than five years before diagnosis.



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Table 3| Estimation of number of melanoma cases attributed to sunbed use in Europe

Incidence case caused by ever use of sunbedsAttributable fraction (%)*

Population TotalWomenMenWomenMen

86523410.66.5Austria†

1431024110.66.5Belgium†

1571065213.08.1Denmark

7243299.45.8Finland‡

203157473.81.4France

140490450010.66.5Germany

3311.30.4Greece§

2116.13.9Iceland

302555.81.6Ireland

6752151.30.4Italy§

64210.66.5Luxembourg†

9557389.45.8Norway‡

8711.30.4Portugal§

322661.30.4Spain

184113719.45.8Sweden

155101548.75.1Switzerland

34523111410.66.5Netherlands†

444357875.81.6United Kingdom

343823411096Total

*Calculated from relative risk determined in present meta-analysis and various surveys on prevalence of sunbed use in population.†Prevalence data for Germany were used for Austria, Luxembourg, Belgium, and Netherlands.‡Prevalence data for Sweden were used for Finland and Norway. As no data were reported for men, we applied the male:female ratio from Germany survey toSweden prevalence data.§Prevalence data for Spain were used for Greece, Italy, and Portugal.



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Figures

Fig 1 Flow of studies on sunbed use and risk of cutaneous melanoma

Fig 2 Forest plot of risk for melanoma associated with ever use of sunbeds. Heterogeneity I²=57% for all studies combined



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Fig 3 Forest plot of risk for melanoma associated with ever use of sunbeds when first use was before age 35 years. Noheterogeneity (I2=0)

Fig 4 Forest plot of risk for melanoma associated with high use of sunbeds. Heterogeneity I²=47%

Fig 5 Risk for melanoma associated with ever use of sunbeds as a function of latitude



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